Centrioles to basal bodies in the spermiogenesis of Mastotermes darwiniensis (Insecta, Isoptera)

Abstract

In addition to their role in centrosome organization, the centrioles have another distinct function as basal bodies for the formation of cilia and flagella. Centriole duplication has been reported to require two alternate assembly pathways: template or de novo. Since spermiogenesis in the termite Mastotermes darwiniensis lead to the formation of multiflagellate sperm, this process represents a useful model system in which to follow basal body formation and flagella assembly. We present evidence of a possible de novo pathway for basal body formation in the differentiating germ cell. This cell also contains typical centrosomal proteins, such as centrosomin, pericentrin-like protein, gamma-tubulin, that undergo redistribution as spermatid differentiation proceeds. The spermatid centrioles are long structures formed by nine doublet rather than triplet microtubules provided with short projections extending towards the surrounding cytoplasm and with links between doublets. The sperm basal bodies are aligned in parallel beneath the nucleus. They consist of long regions close to the nucleus showing nine doublets in a cartwheel array devoid of any projections; on the contrary, the short region close to the plasma membrane, where the sperm flagella emerge, is characterized by projections similar to those observed in the centrioles linking the basal body to the plasma membrane. It is hypothesized that this appearance is in connection with the centriole elongation and further with the flagellar axonemal organization. Microtubule doublets of sperm flagellar axonemes are provided with outer dynein arms, while inner arms are rarely visible.

Evolution and spermatogenesis

“…During spermatogenesis, the developing centrioles transform into basal bodies, providing a template for the growing axoneme. Centrioles normally duplicate during S-phase, but at least in multiflagellate M. darwiniensis, centrioles can be synthesized de novo (Riparbelli et al 2009). Proper formation of the basal body is essential for sperm motility, as has been shown by a mutation in the Drosophila homologue of the evolutionary conserved centriole protein Bld10, which is part of the somatic centriole as well as of the basal body.…”

Structural characterization of procentrioles in Drosophila spermatids

“…Rodent sperm do not contribute at all functional centrioles [Manandhar et al, 1998;Woolley and Fawcett, 1973] and some aflagellate sperm in insects lose their centrioles during spermiogenesis [Dallai, 2014]. By contrast, the multiflagellated sperm cells of the termite Mastotermes darwiniensis (Isoptera) contain hundred centrioles each able to nucleate an axoneme during spermatid differentiation [Baccetti and Dallai, 1978;Riparbelli et al, 2009]. The fate and contribution of these supernumerary centrioles at fertilization remain unknown.…”

The evolution of insect sperm − an unusual character system in a megadiverse group

“…), while about 100 basal bodies are formed in Mastotermes (Blattodea) (Riparbelli et al. ). *Supernumerary procentrioles in spermatocytes: (0) absent; (1) present. Present in Bombyx (Yamashiki and Kawamura ) and also described for Ephestia (Pyralidae) (Wolf and Kyburg ) and Pieris (Pieridae) (Gottardo et al.…”

“…Among animal sperm, the multiflagellate condition with about 100 flagella is unique to Mastotermes (Riparbellim et al. ). Spatial arrangement of axoneme and nucleus : (0) axoneme starting from beneath the nucleus ; (1) partially running parallel with the nucleus . An axoneme running parallel with the nucleus is present in Campodea (Diplura), Acerentomon (Protura), Lepisma (Zygentoma), Haplothrips and other Thysanoptera (Fig.…”